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Microbial Metabolic Rates in the Ross Sea: the ABIOCLEAR Project

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Microbial Metabolic Rates in the Ross Sea: the ABIOCLEAR Project A peer-reviewed open-access journal Nature Conservation 34:Microbial 441–475 (2019)metabolic rates in the Ross Sea: the ABIOCLEAR Project 441 doi: 10.3897/natureconservation.34.30631 RESEARCH ARTICLE http://natureconservation.pensoft.net Launched to accelerate biodiversity conservation Microbial metabolic rates in the Ross Sea: the ABIOCLEAR Project Maurizio Azzaro1, Theodore T. Packard2, Luis Salvador Monticelli1, Giovanna Maimone1, Alessandro Ciro Rappazzo1,3, Filippo Azzaro1, Federica Grilli4, Ermanno Crisafi1, Rosabruna La Ferla1 1 Institute of Polar Science (ISP-CNR Messina), Spianata S. Raineri 86, 98122 Messina, Italy 2 Marine Ecophysiology Group (EOMAR), University of Las Palmas de Gran Canaria, Campus Universitario de Tafira 35017, Las Palmas de Gran Canaria, Spain 3 National Interuniversity Consortium for Marine Sciences (Co- NISMa), Piazzale Flaminio 9, 00196 Roma, Italy 4 Institute for Biological Resources and Marine Biotechno- logies (IRBIM-CNR Ancona), Largo Fiera della Pesca 2, 60125 Ancona, Italy Corresponding author: Rosabruna La Ferla ([email protected]) Academic editor: A. Lugliè | Received 17 October 2018 | Accepted 25 February 2019 | Published 3 May 2019 http://zoobank.org/83471DD2-4EB3-4F6F-A8FA-B02F7117115 Citation: Azzaro M, Packard TT, Monticelli LS, Maimone G, Rappazzo AC, Azzaro F, Grilli F, Crisafi E, La Ferla R (2019) Microbial metabolic rates in the Ross Sea: the ABIOCLEAR Project. In: Mazzocchi MG, Capotondi L, Freppaz M, Lugliè A, Campanaro A (Eds) Italian Long-Term Ecological Research for understanding ecosystem diversity and functioning. Case studies from aquatic, terrestrial and transitional domains. Nature Conservation 34: 441–475. https:// doi.org/10.3897/natureconservation.34.30631 Abstract The Ross Sea is one of the most productive areas of the Southern Ocean and includes several function- ally different marine ecosystems. With the aim of identifying signs and patterns of microbial response to current climate change, seawater microbial populations were sampled at different depths, from surface to the bottom, at two Ross Sea mooring areas southeast of Victoria Land in Antarctica. This oceano- graphic experiment, the XX Italian Antarctic Expedition, 2004-05, was carried out in the framework of the ABIOCLEAR project as part of LTER-Italy. Here, microbial biogeochemical rates of respiration, carbon dioxide production, total community heterotrophic energy production, prokaryotic heterotrophic activity, production (by 3H-leucine uptake) and prokaryotic biomass (by image analysis) were determined throughout the water column. As ancillary parameters, chlorophyll a, adenosine-triphosphate concentra- tions, temperature and salinity were measured and reported. Microbial metabolism was highly variable amongst stations and depths. In epi- and mesopelagic zones, respiratory rates varied between 52.4–437.0 -1 -1 and 6.3–271.5 nanol O2 l h ; prokaryotic heterotrophic production varied between 0.46–29.5 and 0.3–6.11 nanog C l-1 h-1; and prokaryotic biomass varied between 0.8–24.5 and 1.1–9.0 µg C l-1, re- spectively. The average heterotrophic energy production ranged between 570 and 103 mJ l-1 h-1 in upper Copyright Maurizio Azzaro et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 442 Maurizio Azzaro et al. / Nature Conservation 34: 441–475 (2019) and deeper layers, respectively. In the epipelagic layer, the Prokaryotic Carbon Demand and Prokaryotic Growth Efficiency averaged 9 times higher and 2 times lower, respectively, than in the mesopelagic one. The distribution of plankton metabolism and organic matter degradation was mainly related to the differ- ent hydrological and trophic conditions. In comparison with previous research, the Ross Sea results, here, evidenced a relatively impoverished oligotrophic microbial community, throughout the water column. Keywords Microbial respiration, heterotrophic production, heterotrophic energy production, Ross Sea, Antarctica, LTER Introduction The present work aims to explore the carbon fate through microbes in an area of the Ross Sea (RS) and to identify signs and patterns of microbial responses to current climate change. The Southern Ocean (SO) plays an important role in world climate since it is considered the engine of the worldwide oceanic currents. The dramatic seasonal vari- ability in environmental factors in SO generates a significant stress on the biota which must endure constant sunlight, oscillating temperatures and melting ice phenomena in spring-summer time. The annual pelagic primary production is largely confined to this period, when light and nutrient conditions are favourable for the phytoplankton growth. Studies on global change have revealed that the SO is becoming a larger car- bon sink with over 30–40% of total carbon uptake occurring there (Lancelot 2007, Khatiwala et al. 2009). Recently, an early spring retreat of sea ice, along with a decrease in seasonal sea-ice cover, an increase of light availability and a presumed constraint on primary production, has also been reported (Dinasquet et al. 2018, Constable et al. 2014). Furthermore, the low iron-limited primary productivity ensures that SO falls into a high-nutrient low-chlorophyll (HNLC) type of environment (Minas et al. 1986, Dinasquet et al. 2018, Deppler and Davidson 2017). One of the most productive and peculiar area of the SO continental shelf zone is the RS (Nelson et al. 1996). This region (1.55 million km2 of ocean bordering Antarc- tica from ice edge to deep ocean) was established as a Marine Protected Area (MPA) in December 2017. Here, a peculiar and relatively simply trophic web exists. The phy- toplankton, dominated by either diatoms or Phaeocystis sp., depending on whether the euphotic zone is stratified or deeply mixed, is grazed either by krill or silver fish that, in turn, sustain the higher trophic levels (Deppler and Davidson 2017). The RS includes a mosaic of functionally different marine ecosystems mainly linked to sea ice distribution whose variability induces unpredicted cascade effects on trophic dynamics and carbon and nutrient drawdown (Catalano et al. 2006, Smith et al. 2007, Vichi et al. 2009). Accordingly, different fates involve the organic matter transfer, carbon ex- port and depth sequestration. The relevance of high latitude oceans, such as the RS, to models and budgets of global carbon cycling has stimulated recent studies of organic matter degradation in the RS water column (Nelson et al. 1996, Carlson and Hansell 2003, Langone et al. 2003, Azzaro et al. 2006, Misic et al. 2017). Microbial metabolic rates in the Ross Sea: the ABIOCLEAR Project 443 Catalano et al. (2006) confirmed that, in spring-summer periods, about 90% of the total carbon derived from new production was exported via higher trophic levels. Comparing the oxidation and sinking of organic matter through the deep water found that, according to sediment-traps estimates, 63% of organic carbon, remineralized to CO2 by microbial respiration, originated in the particulate organic matter (POC) pool (Azzaro et al. 2006). Such evidence highlighted POC as the main organic fuel in the RS biological pump. The oxidation rate, fuelling the dissolved organic fraction, was not measured by sediment traps (Jiao et al. 2010, Legendre et al. 2015), but it was a smaller fraction, here in the RS, than it was in other oceans (Azzaro et al. 2006). Although microbes constitute the sentinel of ecosystem evolution (Dutta and Du- tta 2016), to date, relatively little is known in the RS about the microbial contribution to the degradation of the carbon pool. Amongst the biological processes and meta- bolic activities, respiration has particularly been neglected despite its great impact on environmental ecology (Packard 2017). Respiration is controlled by the respiratory electron transport system activity (ETS) in all organisms on the planet (Packard 1969, Packard et al. 1971, Lane 2006, Packard et al. 2015). It functions in aerobic and an- aerobic conditions, as well as in extreme or deep marine environments (Koppelmann et al. 2004, Azzaro et al. 2006, Packard and Codispoti 2007, Baltar et al. 2010). The ETS assay was originally designed by Packard (1971). The biochemical relationship amongst the biological energy currency, adenosine triphosphate (ATP) and ETS was completely unknown before the 1940s. In few words, in all living organisms, during cellular respiration, the electron transport system produces the bulk of the cell energy in the form of ATP molecules. However, earlier, the idea of capturing biologically us- able energy from respiration was appreciated by the biophysicist, Alfred Lotka (1925). He felt that Darwinian natural selection was the result of competition between or- ganisms for energy. Those individuals that extracted, stored and used energy most ef- ficiently survived and reproduced more often than their competitors. Building on this concept, Howard Odum described energy flow in freshwater streams (Odum 1956). David Karl recently argued that biological energy production in the ocean should be assessed to understand ocean productivity better (Karl 2014). Still, none of the earlier work calculated energy production from the biochemical processes that produce this energy. They used distantly related proxies such as biomass or, the more related one, heat production (Pamatmat et al. 1981).
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